A major problem in evolutionary theory is to explain the widespread occurrence of sexual recombination. This is particularly difficult in anisogamous species where the familiar 'two-fold cost of sex' is encountered. Another cost has recently been identified: that fusion of gametes allows intracellular parasites or deleterious 'selfish' genomes to invade a population. These costs of anisogamy and the ability of cytoplasmic agents to invade a sexual population are quantified, allowing the costs and consequences of different modes of reproduction to be compared. It is found that the costs of selfish elements are likely to be very high and, in particular, that isogamous sexual reproduction (the putative 'primitive' form) is not cost-free, but incurs a fitness reduction of the order of 90%; thus a large selective disadvantage occurs in the initial evolution of sex which is ignored in standard analysis. Even once anisogamy has evolved, the low levels of 'paternal leakage' observed in many extant organisms may allow selfish cytoplasmic elements to spread, resulting in moderate to large decreases in host population fitness. However, much of the cost of selfish elements is avoided in sexual lifecycles with a large number of asexual cellular divisions between sexual reproduction: this greatly impedes the spread of selfish agents and reduces the fitness loss attributable to selfish elements.
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